Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch

Abstract

. Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch. Am J Physiol Renal Physiol 291: F770 -F780, 2006. First published April 11, 2006 doi:10.1152/ajprenal.00026.2006.-Marine elasmobranchs maintain internal osmolality higher than their external environment, resulting in an osmotic gradient for branchial water uptake. This gradient is markedly increased in low-salinity habitats. The subsequent increase in water uptake presents a challenge to volume homeostasis. The Atlantic stingray is a marine elasmobranch that inhabits a remarkable range of environmental salinities. We hypothesized that the ability of these stingrays to regulate fluid volume in low-salinity environments is due primarily to a renal glomerular and tubular functional reserve. We tested this hypothesis by measuring renal excretory function after a rapid and sustained 50% reduction in the osmolality of the external medium. Atlantic stingrays were maintained in harbor water [control salinity (CS) ϳ850 mosmol/kgH 2O] for 1 wk. Rays were then either transferred to diluted harbor water [low salinity (LS) ϳ440 mosmol/kgH 2O] or maintained in CS for a further 24 h. Renal excretory function was markedly higher in the rays subjected to low salinity. Glomerular filtration rate was threefold higher and urine flow rate ninefold higher in the LS group. The clearance of solute-free water was greater, and solute-free water comprised a significantly larger proportion of the urine output for the stingrays transferred to dilute harbor water. We conclude that 1) the kidneys of Atlantic stingrays have a remarkable glomerular and tubular functional reserve, and 2) the marked increase in renal function attenuates the increase in fluid volume when these fish move into low-salinity habitats. free water clearance; glomerular filtration rate; tubular urea reabsorption IN GENERAL, MARINE ELASMOBRANCH fishes (sharks, skates, and rays) maintain body fluids hyperosmotic to the ambient environment as part of their osmo-and volume-regulatory strategies. In the ocean, for example, plasma osmolality is 2-10% higher than the osmolality of the surrounding seawater (for review, see Ref. 28), this being due to their ability to maintain high Na ϩ , Cl Ϫ , and urea concentrations in the extracellular fluid (for review, see Refs. 28 and 51).Most species of marine elasmobranchs are confined to marine habitats (9) and only encounter relatively small variations in environmental salinity. However, some species are found in estuaries, as well as marine environments, and therefore can be considered marginally euryhaline (9). Furthermore, a small number of species are euryhaline; i.e., they are able to reside in marine, estuarine, riverine, and even freshwater habitats for extended periods of time. Although, these euryhaline elasmobranchs appear to migrate between habitats on a seasonal basis (48, 54), at least one species, the Atlantic stingray, Dasyatis sabina, can reproduce and complete its life cycle in freshwat...

Proteomic and physiological responses of leopard sharks (Triakis semifasciata) to salinity change

“…The hematological results revealed no effect of salinity on HCT or RBC characteristics, as found in other elasmobranch studies (e.g. Janech et al, 2006;Sulikowski et al, 2003). Similarly, plasma concentrations of sodium, chloride and potassium ions either remained unchanged or stabilized at new, lower levels by 48 h that persisted over the 3 weeks.…”

“…Given that leopard sharks are very rarely captured near or below 50% SW, our data are consistent with the hypotheses that partially euryhaline sharks cannot switch from net ion excretion to net ion uptake and also cannot defend large hyperosmotic gradients. These physiological limitations contrast with the abilities of truly euryhaline elasmobranchs in FW (Janech et al, 2006;Pillans and Franklin, 2004;Pillans et al, 2005). It is possible that partially euryhaline elasmobranchs simply cannot regulate the abundances or activities of necessary epithelial transporters when facing dilute salinity.…”

Branchial osmoregulation in the euryhaline bull shark, Carcharhinus leucas: a molecular analysis of ion transporters

“…Moreover, in the stenohaline FW stingrays Potamotrygon spp., the gland is greatly atrophied and is non-functional (Thorson et al, 1978). The kidneys are important for effective osmoregulation in FW, producing a large volume of urine in response to osmotic water gain, while also facilitating tubular reabsorption of urea and Na + and Cl -ions to reduce urinary osmolyte losses (Payan et al, 1973;Janech and Piermarini, 2002;Janech et al, 2006). The modulation of hepatic urea production is also critical for euryhaline elasmobranchs to maintain plasma osmolality as appropriate with changes in environmental salinity (Tam et al, 2003;Anderson et al, 2005).…”

Cloning and functional characterization of a second urea transporter from the kidney of the Atlantic stingray,Dasyatis sabina

“…The lower expression of the 5.5-kb strUT-2c transcript indicates that the long 3ЈUTR splice variant of strUT-2 may be selectively downregulated during acute dilution. Although there are discontinuities between UT RNA and protein abundance (1,46), if strUT protein abundance changes in parallel with strUT RNA levels, the acute decrease in fractional urea reabsorption reported for stingrays in dilute seawater (19) could result, at least in part, from downregulation of strUT-2 expression following a decrease in strUT-2c mRNA abundance.…”

“…Buffered harbor water was added to the control tank. The animals were held for an additional 24 h, under conditions similar to those described previously (19). Animals were then anesthetized by placement in buffered (pH 8.0 -8.3) sea water containing MS-222 (aminobenzoic acid ethyl ester, Sigma, St. Louis, MO).…”